Theta oscillation-coupled dendritic spiking integrates inputs on a long time scale

Hippocampus

Volumn 15, Issue 7, 2005, Pages 950-962

  Huhn, Zsófia ^a   Orbán, Gergo ^a,b   Érdi, Péter ^a,c   Lengyel, Máté ^d  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b INSTITUTE FOR ADVANCED STUDY   (Hungary)

^c KALAMAZOO COLLEGE   (United States)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Active dendrites; Persistent activity; Phase precession; Place cells; Working memory

Indexed keywords

ACTION POTENTIAL; ARTICLE; CELL MEMBRANE DEPOLARIZATION; COMPARTMENT MODEL; CONTROLLED STUDY; DENDRITE; HIPPOCAMPUS; HIPPOCAMPUS THETA RHYTHM; MENTAL TASK; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL STIMULATION; OSCILLATION; PERCEPTIVE THRESHOLD; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SPIKE; WORKING MEMORY;

ACTION POTENTIALS; ANIMALS; BIOLOGICAL CLOCKS; DENDRITES; HIPPOCAMPUS; HUMANS; MEMORY, SHORT-TERM; NEURAL NETWORKS (COMPUTER); PYRAMIDAL CELLS; RATS; REACTION TIME; SYNAPTIC TRANSMISSION; THETA RHYTHM; TIME FACTORS;

EID: 27644550644     PISSN: 10509631     EISSN: None     Source Type: Journal    
DOI: 10.1002/hipo.20112     Document Type: Article

References (94)

1. Andrade R. 1991. Cell excitation enhances muscarinic cholinergic responses in rat association cortex. Brain Res 548:81-93.
2. Baeg EH, Kim YB, Huh K, Mook-Jung I, Kim HT, Jung MW. 2003. Dynamics of population code for working memory in the prefrontal cortex. Neuron 40:177-188.
3. Bernander O, Douglas RJ, Martin KA, Koch C. 1991. Synaptic background activity influences spatiotemporal integration in single pyramidal cells. Proc Natl Acad Sci USA 88:11569-11573.
4. Brody CD, Hernandez A, Zainos A, Romo R. 2003. Timing and neural encoding of somatosensory parametric working memory in macaque prefrontal cortex. Cereb Cortex 13:1196-1207.
5. Burgess N, Recce M, O'Keefe J. 1994. A model of hippocampal function. Neural Netw 7:1065-1081.
6. Buzsáki G. 2002. Theta oscillations in the hippocampus. Neuron 33:325-340.
7. Buzsáki G, Draguhn A. 2004. Neuronal oscillations in cortical networks. Science 304:1926-1929.
8. Cook EP, Johnston D. 1997. Active dendrites reduce location dependent variability of synaptic input trains. J Neurophysiol 78:2116-2128.
9. Csicsvári J, Hirase H, Czurkó A, Mamiya A, Buzsáki G. 1999. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J Neurosci 19:274-287.
10. Deadwyler SA, Hampson RE. 2004. Differential but complementary mnemonic functions of the hippocampus and subiculum. Neuron 42:465-476.
11. Destexhe A, Pare D. 1999. Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. J Neurophysiol 81:1531-1547.
12. Destexhe A, Mainen ZF, Sejnowski TJ. 1998. Kinetic models of synaptic transmission. In: Koch C, Segev I, editors. Methods in neuronal modeling. 2nd ed. Cambridge, MA: MIT Press/A Bradford Book. p 251-291.
13. Destexhe A, Rudolph M, Paré D. 2003. The high-conductance state of neocortical neurons in vivo. Nat Rev Neurosci 4:739-751.
14. Egorov AV, Hamam BN, Fransen E, Hasselmo ME, Alonso AA. 2002. Graded persistent activity in entorhinal cortex neurons. Nature 420:173-178.
15. Ermentrout B. 1996. Type I membranes, phase resetting curves, and synchrony. Neural Comput 8:979-1001.
16. Fell J, Klaver P, Elfadil H, Schaller C, Elger CE, Fernandez G. 2003. Rhinalhippocampal theta coherence during declarative memory formation: interaction with gamma synchronization? Eur J Neurosci 17:1082-1088.
17. Fox SE. 1989. Membrane potential and impedance changes in hippocampal pyramidal cells during theta rhythm. Exp Brain Res 77:283-294.
18. Frank LM, Brown EN, Wilson MA. 2001. A comparison of the firing properties of putative excitatory and inhibitory neurons from CA1 and the entorhinal cortex. J Neurophysiol 86:2029-2040.
19. Fransen E, Alonso AA, Hasselmo ME. 2002. Simulations of the role of muscarinic-activated calcium-sensitive nonspecific cation current INCM in entorhinal neuronal activity during delayed matching tasks. J Neurosci 22:1081-1097.
20. Freund TF, Buzsáki G. 1996. Interneurons of the hippocampus. Hippocampus 6:347-470.
21. Fuster JM. 2001. The prefrontal cortex-an update: time is of the essence. Neuron 30:319-333.
22. Gevins A, Smith ME, McEvoy L, Yu D. 1997. High-resolution EEG mapping of cortical activation related to working memory: effects of task difficulty, type of processing, and practice. Cereb Cortex 7:374-385.
23. Gillies MJ, Traub RD, LeBeau FE, Davies CH, Gloveli T, Buhl EH, Whittington MA. 2002. A model of atropine-resistant theta oscillations in rat hippocampal area CA1. J Physiol 543:779-793.
24. Givens BS. 1996. Stimulus-evoked resetting of the dentate theta rhythm: relation to working memory. Neuroreport 8:159-163.
25. Givens BS, Olton DS. 1990. Cholinergic and GABAergic modulation of medial septal area: effect on working memory. Behav Neurosci 104:849-855.
26. Gold JI, Shadlen MN. 2002. Banburismus and the brain: decoding the relationship between sensory stimuli, decisions, and rewards. Neuron 36:299-308.
27. Golding NL, Spruston N. 1998. Dendritic sodium spikes are variable triggers of axonal action potentials in hippocampal CA1 pyramidal neurons. Neuron 21:1189-1200.
28. Golding NL, Staff NP, Spruston N. 2002. Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 418:326-331.
29. Goldman MS, Levine JH, Major G, Tank DW, Seung HS. 2003. Robust persistent neural activity in a model integrator with multiple hysteretic dendrites per neuron. Cereb Cortex 13:1185-1195.
30. Harris KD, Henze DA, Hirase H, Leinekugel X, Dragoi G, Czurkó A, Buzsáki G. 2002. Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature 417:738-741.
31. Hasselmo ME, Bodelon C, Wyble BP. 2002. A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comput 14:793-817.
32. Hausser M, Spruston N, Stuart GJ. 2000. Diversity and dynamics of dendritic signaling. Science 290:739-744.
33. Helmchen F, Fee MS, Tank DW, Denk W. 2001. A miniature head-mounted two photon microscope. High-resolution brain imaging in freely moving animals. Neuron 31:903-912.
34. Huxter J, Burgess N, O'Keefe J. 2003. Independent rate and temporal coding in hippocampal pyramidal cells. Nature 425:828-832.
35. Jensen O, Lisman JE. 1996. Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells. Learn Mem 3:279-287.
36. Jensen O, Lisman JE. 1998. An oscillatory short-term memory buffer model can account for data on the Sternberg task. J Neurosci 18:10688-10699.
37. Jensen O, Lisman JE. 2005. Hippocampal sequence-encoding driven by a cortical multiitem working memory buffer. Trends Neurosci 28:67-72.
38. Jensen O, Tesche CD. 2002. Frontal theta activity in humans increases with memory load in a working memory task. Eur J Neurosci 15:1395-1399.
39. Jensen O, Idiart M, Lisman JE. 1996. Physiologically realistic formation of autoassociative memory in networks with theta/gamma oscillations: role of fast NMDA channels. Learn Mem 3:243-256.
40. Kahana MJ, Seelig D, Madsen JR. 2001. Theta returns. Curr Opin Neurobiol 11:739-744.
41. Kamondi A, Acsády L, Wang XJ, Buzsáki G. 1998. Theta oscillation in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase precession of action potentials. Hippocampus 8:244-261.
42. Klausberger T, Magill PJ, Márton LF, Roberts JD, Cobden PM, Buzsáki G, Somogyi P. 2003. Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421:844-848.
43. Mink R, Alonso AA. 1997. Ionic mechanisms of muscarinic depolarization in entorhinal cortex layer II neurons. J Neurophysiol 77:1829-1843.
44. Koulakov AA, Raghavachari S, Kepecs A, Lisman JE. 2002. Model for a robust neural integrator. Nat Neurosci 5:775-782.
45. Lee H, Simpson GV, Logothetis NK, Rainer G. 2005. Phase locking of single neuron activity to theta oscillations during working memory in monkey extrastriate visual cortex. Neuron 45:147-156.
46. Lengyel M, Érdi P. 2004. Theta modulated feed-forward network generates rate and phase coded firing in the entorhino-hippocampal system. IEEE Trans Neural Netw 15:1092-1099.
47. Lengyel M, Szatmáry Z, Érdi P. 2003. Dynamically detuned oscillations account for the coupled rate and temporal code of place cell firing. Hippocampus 13:700-714.
48. Leung LS, Yim CY. 1986. Intracellular records of theta rhythm in hippocampal CA1 cells of the rat. Brain Res 367:323-327.
49. Lisman JE, Idiart MAP. 1995. Storage of 7 ± 2 short-term memories in oscillatory subcycles. Science 267:1512-1515.
50. Machens CK, Romo R, Brody CD. 2005. Flexible control of mutual inhibition: a neural model of two-interval discrimination. Science 307:1121-1124.
51. Macrides F, Eichenbaum HB, Forbes WB. 1982. Temporal relationship between sniffing and the limbic theta rhythm during odor discrimination reversal learning. J Neurosci 2:1705-1717.
52. Magee J, Hoffman D, Colbert C, Johnston D. 1998. Electrical and calcium signaling in dendrites of hippocampal pyramidal neurons. Annu Rev Physiol 60:327-346.
53. h normalizes temporal summation in hippocampal CA1 neurons. Nat Neurosci 2:508-514.
54. Major G, Tank D. 2004. Persistent neural activity: prevalence and mechanisms. Curr Opin Neurobiol 14:675-684.
55. Marder E, Abbott LF, Turrigiano GG, Liu Z, Golowasch J. 1996. Memory from the dynamics of intrinsic membrane currents. Proc Natl Acad Sci USA 93:13481-13486.
56. McNaughton BL, Barnes CA, Gerrard JL, Gothard K, Jung MW, Knierim JJ, Kudrimoti H, Qin Y, Skaggs WE, Suster M, Weaver KL. 1996. Deciphering the hippocampal polyglott: the hippocampus as a path integration system. J Exp Biol 199:173-185.
57. Mehra MR, Lee AK, Wilson MA. 2002. Role of experience and oscillations in transforming a rate code into a temporal code. Nature 417:741-746.
58. Mizuhara H, Wang LQ, Kobayashi K, Yamaguchi Y. 2004. A long-range cortical network emerging with theta oscillation in a mental task. Neuroreport 15:1233-1238.
59. Mizumori SJ, Perez GM, Alvado MC, Barnes CA, McNaughton BL. 1990. Reversible inactivation of the medial septum differentially affects two forms of learning in rats. Brain Res 528:12-20.
60. O'Keefe J, Dostrovsky J. 1971. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely moving rat. Brain Res 34:171-175.
61. O'Keefe J, Recce ML. 1993. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317-330.
62. Pan WX, McNaughton N. 1997. The medial supramammillary nucleus, spatial learning and the frequency of hippocampal theta activity. Brain Res 764:101-108.
63. Pinsky PF, Rinzel J. 1994. Intrinsic and network rythmogenesis in a reduced Traub model for CA3 neurons. J Comput Neurosci 1:39-60.
64. Poirazi P, Brannon T, Mel BW. 2003. Pyramidal neuron as two-layer neural network. Neuron 37:989-999.
65. Rall W. 1959. Branching dendritic trees and motoneuron membrane resistivity. Exp Neurol 1:491-527.
66. Rall W. 1989. Cable theory for dendritic neurons. In: Koch C, Segev I, editors. Methods in neuronal modeling. Cambridge, MA: The MIT Press. p 29-38.
67. Redish AD, Touretzky DS. 1997. Cognitive maps beyond the hippocampus. Hippocampus 7:15-35.
68. Redish AD, McNaughton BL, Barnes CA. 2000. Place cell firing shows an inertia-like process. Neurocomputing 32-33:235-241.
69. Reyes A. 2001. Influence of dendritic conductances on the input-output properties of neurons. Annu Rev Neurosci 24:653-675.
70. Rudolph M, Destexhe A. 2003a. A fast-conducting, stochastic integrative mode for neocortical neurons in vivo. J Neurosci 23:2466-2476.
71. Rudolph M, Destexhe A. 2003b. Tuning neocortical pyramidal neurons between integrators and coincidence detectors. J Comput Neurosci 14:239-251.
72. Samsonovich A, McNaughton BL. 1997. Path integration and cognitive mapping in a continuous attractor neural network model. J Neurosci 17:5900-5920.
73. Sarnthein J, Petsche H, Rappelsberger P, Shaw GL, von Stein A. 1998. Synchronization between prefrontal and posterior association cortex during human working memory. Proc Natl Acad Sci USA 95:7092-7096.
74. Sauseng P, Klimesch W, Doppelmayr M, Hanslmayr S, Schabus M, Gruber WR. 2004. Theta coupling in the human electroencephalogram during a working memory task. Neurosci Lett 354:123-126.
75. Seidenbecher T, Laxmi TR, Stork O, Pape HC. 2003. Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval. Science 301:846-850.
76. Seung HS. 1996. How the brain keeps the eyes still. Proc Natl Acad Sci USA 93:13339-13344.
77. Sharp PE. 1997. Subicular cells generate similar spatial firing patterns in two geometrically and visually distinctive environments: comparison with hippocampal place cells. Behav Brain Res 85:71-92.
78. Skaggs WE, McNaughton BL, Wilson MA, Barnes CA. 1996. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6:149-172.
79. Soltész I, Deschenes M. 1993. Low and high-frequency membrane potential oscillations during theta activity in CA1 and CA3 pyramidal neurons of the rat hippocampus under ketamine-xylazine anesthesia. J Neurophysiol 70:97-116.
80. Spencer WA, Kandel ER. 1961. Electrophysiology of hippocampal neurons. IV. Fast prepotentials. J Neurophysiol 24:272-285.
81. Stam CJ, van Cappellen van Walsum AM, Micheloyannis S. 2002. Variability of EEG synchronization during a working memory task in healthy subjects. Int J Psychophysiol 46:53-66.
82. Tesche CD, Karhu J. 2000. Theta oscillations index human hippocampal activation during a working memory task. Proc Natl Acad Sci USA 97:919-924.
83. Tsodyks MV, Skaggs WE, Sejnowski TJ, McNaughton BL. 1996. Population dynamics and theta phase precession of hippocampal place cell firing: a spiking neuron model. Hippocampus 6:271-280.
84. Vanderwolf CH. 1969. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26:407-418.
85. Vetter P, Roth A, Hausser M. 2001. Propagation of action potentials in dendrites depends on dendritic morphology. J Neurophysiol 85:926-937.
86. Wallenstein GV, Hasselmo ME. 1997. GABAergic modulation of hippocampal activity: sequence learning, place field development, and the phase precession effect. J Neurophysiol 78:393-408.
87. Williams SR. 2004. Spatial compartmentalization and functional impact of conductance in pyramidal neurons. Nat Neurosci 7:961-967.
88. Williams SR, Stuart GJ. 2003. Role of dendritic synapse location in the control of action potential output. Trends Neurosci 26:146-154.
89. Winson J. 1978. Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. Science 201:160-163.
90. Wong RK, Prince DA, Basbaum AI. 1979. Intradendritic recordings from hippocampal neurons. Proc Natl Acad Sci USA 76:986-990.
91. Yamaguchi Y. 2003. A theory of hippocampal memory based on theta phase precession. Biol Cybern 89:1-9.
92. Yamaguchi Y, Aota Y, McNaughton BL, Lipa P. 2002. Bimodality of theta phase precession in hippocampal place cells in freely running rats. J Neurophysiol 87:2639-2642.
93. Ylinen A, Soltész I, Bragin A, Penttonen M, Sík A, Buzsáki G. 1995. Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells, and basket cells. Hippocampus 5:78-90.
94. Zugaro MB, Monconduit L, Buzsáki G. 2005. Spike phase precession persists after transient intrahippocampal perturbation. Nat Neurosci 8:67-71.